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An adaptive epigenetic memory in conifers with important implications for seed production

Published online by Cambridge University Press:  24 January 2012

Igor Yakovlev ,
Carl Gunnar Fossdal ,
Tore Skrøppa ,
Jorunn E. Olsen ,
Anne Hope Jahren  and
Øystein Johnsen
Igor Yakovlev*
Affiliation:
Norwegian Forest and Landscape Institute, PO Box 115, N-1431, Ås, Norway
Carl Gunnar Fossdal
Affiliation:
Norwegian Forest and Landscape Institute, PO Box 115, N-1431, Ås, Norway
Tore Skrøppa
Affiliation:
Norwegian Forest and Landscape Institute, PO Box 115, N-1431, Ås, Norway
Jorunn E. Olsen
Affiliation:
Department of Plant and Environmental Sciences, Norwegian University of Life Sciences, N-1432, Ås, Norway
Anne Hope Jahren
Affiliation:
School of Ocean and Earth Science and Technology, University of Hawaii, Honolulu, HI 96822, USA
Øystein Johnsen
Affiliation:
Department of Plant and Environmental Sciences, Norwegian University of Life Sciences, N-1432, Ås, Norway
*
*Correspondence Email: [email protected]
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Abstract

Conifers are evolutionarily more ancient than their angiosperm counterparts, and thus some adaptive mechanisms and features influenced by epigenetic mechanisms appear more highly displayed in these woody gymnosperms. Conifers such as Norway spruce have very long generation times and long life spans, as well as large genome sizes. This seemingly excessive amount of genomic DNA without apparent duplications could be a rich source of sites for epigenetic regulation and modifications. In Norway spruce, an important adaptive mechanism has been identified, called epigenetic memory. This affects the growth cycle of these trees living in environments with mild summers and cold winters, allowing them to adapt rapidly to new and/or changing environments. The temperature during post-meiotic megagametogenesis and seed maturation epigenetically shifts the growth cycle programme of the embryos. This results in significant and long-lasting phenotypic change in the progeny, such as advance or delay of vital phenological processes of high adaptive value, like bud break and bud set. This phenomenon is not only of important evolutionary significance but has clear practical implications for forest seed production and conservation of forest genetic resources. The underlying molecular mechanism that causes the ‘memory’ in long-lived woody species is currently under investigation. Here we summarize the information related to epigenetic memory regulation in gymnosperms, with special emphasis on conifers. The molecular mechanism behind this is still unknown but transcriptional changes are clearly involved. Epigenetic regulation may be realized through several mechanisms, including DNA methylation, histone modification, chromatin remodelling, small non-coding RNAs and transposable element regulation, of which non-coding RNAs might be one of the most important determinants.

Keywords

adaptationchromatin remodellingconifersDNA methylationepigeneticsgenome sizehistone modificationsmegagametogenesissmall RNAstransposable element
Type
Review Papers
Information
Seed Science Research , Volume 22 , Issue 2 , June 2012 , pp. 63 - 76
Copyright
Copyright © Cambridge University Press 2012

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References

Ahuja, M.R. and Neale, D.B. (2005) Evolution of genome size in conifers. Silvae Genetica 54, 126–137.CrossRefGoogle Scholar
Almeida, R. and Allshire, R.C. (2005) RNA silencing and genome regulation. Trends in Cell Biology 15, 251–258.CrossRefGoogle ScholarPubMed
Alvarez, M.E., Nota, F. and Cambiagno, D.A. (2010) Epigenetic control of plant immunity. Molecular Plant Pathology 11, 563–576.CrossRefGoogle ScholarPubMed
Angers, B., Castonguay, E. and Massicotte, R. (2010) Environmentally induced phenotypes and DNA methylation: How to deal with unpredictable conditions until the next generation and after. Molecular Ecology 19, 1283–1295.CrossRefGoogle ScholarPubMed
Axtell, M.J. and Bartel, D.P. (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell 17, 1658–1673.CrossRefGoogle ScholarPubMed
Axtell, M.J. and Bowman, J.L. (2008) Evolution of plant microRNAs and their targets. Trends in Plant Science 13, 343–349.CrossRefGoogle ScholarPubMed
Baroux, C., Pien, S. and Grossniklaus, U. (2007) Chromatin modification and remodeling during early seed development. Current Opinion in Genetics and Development 17, 473–479.CrossRefGoogle ScholarPubMed
Bird, A. (2007) Perceptions of epigenetics. Nature 447, 396–398.CrossRefGoogle ScholarPubMed
Bjørnstad, Å. (1981) Photoperiodical after-effect of parent plant environment in Norway spruce (Picea abies (L.) Karst.) seedlings. Meddelelser fra Norsk Institutt for Skogforskning 36.6, 30s.Google Scholar
Black, J.C. and Whetstine, J.R. (2011) Chromatin landscape: methylation beyond transcription. Epigenetics 6, 13–19.CrossRefGoogle ScholarPubMed
Bock, C. and Lengauer, T. (2008) Computational epigenetics. Bioinformatics 24, 1–10.CrossRefGoogle ScholarPubMed
Bourc'his, D. and Voinnet, O. (2010) A small-RNA perspective on gametogenesis, fertilization, and early zygotic development. Science 330, 617–622.CrossRefGoogle ScholarPubMed
Boyko, A. and Kovalchuk, I. (2010) Transgenerational response to stress in Arabidopsis thaliana. Plant Signaling and Behavior 5, 995–998.CrossRefGoogle ScholarPubMed
Boyko, A., Blevins, T., Yao, Y., Golubov, A., Bilichak, A., Ilnytskyy, Y., Hollander, J., Meins, F. Jr and Kovalchuk, I. (2010) Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of dicer-like proteins. PLoS ONE 5, e9514.CrossRefGoogle ScholarPubMed
Cantino, P.D., Judd, W.S., Soltis, D.E., Omstead, R.G. and Graham, S.W. (2007) Towards a phylogenetic nomenclature of Tracheophyta. Taxon 56, 822–846.CrossRefGoogle Scholar
Carthew, R.W. and Sontheimer, E.J. (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642–655.CrossRefGoogle ScholarPubMed
Chambel, M.R., Climent, J., Alia, R. and Valladares, F. (2005) Phenotypic plasticity: a useful framework for understanding adaptation in forest species. Investigación agraria: Sistemas y recursos forestales 14, 334–344.Google Scholar
Chen, K. and Rajewsky, N. (2007) The evolution of gene regulation by transcription factors and microRNAs. Nature Reviews Genetics 8, 93–103.CrossRefGoogle ScholarPubMed
Chen, M., Lv, S. and Meng, Y. (2010) Epigenetic performers in plants. Development, Growth and Differentiation 52, 555–566.CrossRefGoogle ScholarPubMed
Chinnusamy, V. and Zhu, J.-K. (2009) Epigenetic regulation of stress responses in plants. Current Opinion in Plant Biology 12, 133–139.CrossRefGoogle ScholarPubMed
Costa, F.F. (2008) Non-coding RNAs, epigenetics and complexity. Gene 410, 9–17.CrossRefGoogle ScholarPubMed
Dolgosheina, E.V., Morin, R.D., Aksay, G., Sahinalp, S.C., Magrini, V., Mardis, E.R., Mattsson, J. and Unrau, P.J. (2008) Conifers have a unique small RNA silencing signature. RNA 14, 1508–1515.CrossRefGoogle ScholarPubMed
Dormling, I. and Johnsen, Ø. (1992) Effects of the parental environment on full-sib families of Pinus sylvestris. Canadian Journal of Forest Research 22, 88–100.CrossRefGoogle Scholar
EC (2000) Council Directive 1999/105/EC of 22 December 1999 on the marketing of forest reproductive material. Official Journal of the European Communities L11 43, 17–40.Google Scholar
Feng, S. and Jacobsen, S.E. (2011) Epigenetic modifications in plants: an evolutionary perspective. Current Opinion in Plant Biology 14, 179–186.CrossRefGoogle ScholarPubMed
Fraga, M., Cañal, M. and Rodríguez, R. (2002a) Phase-change related epigenetic and physiological changes in Pinus radiata d. Don. Planta 215, 672–678.CrossRefGoogle ScholarPubMed
Fraga, M.F., Rodríguez, R. and Cañal, M.J. (2002b) Genomic DNA methylation–demethylation during aging and reinvigoration of Pinus radiata. Tree Physiology 22, 813–816.CrossRefGoogle ScholarPubMed
Fuchs, J., Jovtchev, G. and Schubert, I. (2008) The chromosomal distribution of histone methylation marks in gymnosperms differs from that of angiosperms. Chromosome Research 16, 891–898.CrossRefGoogle Scholar
Furner, I.J. and Matzke, M. (2011) Methylation and demethylation of the Arabidopsis genome. Current Opinion in Plant Biology 14, 137–141.CrossRefGoogle ScholarPubMed
Gehring, M. and Henikoff, S. (2007) DNA methylation dynamics in plant genomes. Biochimica et Biophysica Acta (BBA) – Gene Structure and Expression 1769, 276–286.CrossRefGoogle ScholarPubMed
Ginsburg, S. and Jablonka, E. (2009) Epigenetic learning in non-neural organisms. Journal of Biosciences 34, 633–646.CrossRefGoogle ScholarPubMed
Goh, C.-H., Nam, H.G. and Park, Y.S. (2003) Stress memory in plants: a negative regulation of stomatal response and transient induction of rd22 gene to light in abscisic acid-entrained Arabidopsis plants. The Plant Journal 36, 240–255.CrossRefGoogle ScholarPubMed
Grant-Downton, R.T. and Dickinson, H.G. (2006) Epigenetics and its implications for plant biology 2. The ‘epigenetic epiphany’: epigenetics, evolution and beyond. Annals of Botany 97, 11–27.CrossRefGoogle ScholarPubMed
Greenwood, M.S. and Hutchison, K.W. (1996) Genetic aftereffects of increased temperature in Larix. pp. 56–62 in Hom, J.; Birdsey, R.; O'Brian, K. (Eds) Proceedings of the 1995 meeting of the northern global change program. Radnor, USDA Forest Service Report.Google Scholar
Grini, P.E., Thorstensen, T., Alm, V., Vizcay-Barrena, G., Windju, S.S., Jørstad, T.S., Wilson, Z.A. and Aalen, R.B. (2009) The ash1 homolog 2 (ashh2) histone h3 methyltransferase is required for ovule and anther development in Arabidopsis. PLoS ONE 4, e7817.CrossRefGoogle ScholarPubMed
Grotkopp, E., Rejmánek, M., Sanderson, M.J. and Rost, T.L. (2004) Evolution of genome size in pines (Pinus) and its life-history correlates: supertree analyses. Evolution 58, 1705–1729.Google ScholarPubMed
Hamberger, B., Hall, D., Yuen, M., Oddy, C., Hamberger, B., Keeling, C., Ritland, C., Ritland, K. and Bohlmann, J. (2009) Targeted isolation, sequence assembly and characterization of two white spruce (Picea glauca) bac clones for terpenoid synthase and cytochrome p450 genes involved in conifer defence reveal insights into a conifer genome. BMC Plant Biology 9, 106.CrossRefGoogle ScholarPubMed
Hänninen, H., Slaney, M. and Linder, S. (2007) Dormancy release of Norway spruce under climatic warming: testing ecophysiological models of bud burst with a whole-tree chamber experiment. Tree Physiology 27, 291–300.CrossRefGoogle ScholarPubMed
Henderson, I.R. and Jacobsen, S.E. (2007) Epigenetic inheritance in plants. Nature 447, 418–424.CrossRefGoogle ScholarPubMed
Heo, J.B. and Sung, S. (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76–79.CrossRefGoogle ScholarPubMed
Hollick, J.B. (2008) Sensing the epigenome. Trends in Plant Science 13, 398–404.CrossRefGoogle ScholarPubMed
Jablonka, E. and Raz, G. (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. The Quarterly Review of Biology 84, 131–176.CrossRefGoogle Scholar
Jenuwein, T. and Allis, C.D. (2001) Translating the histone code. Science 293, 1074–1080.CrossRefGoogle ScholarPubMed
Johnsen, Ø. (1989a) Phenotypic changes in progenies of northern clones of Picea abies (L.) Karst. grown in a southern seed orchard. I. Frost hardiness in a phytotron experiment. Scandinavian Journal of Forest Research 4, 317–330.CrossRefGoogle Scholar
Johnsen, Ø. (1989b) Phenotypic changes in progenies of northern clones of Picea abies (L.) Karst. grown in a southern seed orchard. II. Seasonal growth rhythm and height in field trials. Scandinavian Journal of Forest Research 4, 331–341.CrossRefGoogle Scholar
Johnsen, Ø., Skrøppa, T., Junttila, O. and Dæhlen, O.G. (1996) Influence of the female flowering environment on autumn frost-hardiness of Picea abies progenies. Theoretical and Applied Genetics 92, 797–802.CrossRefGoogle ScholarPubMed
Johnsen, Ø., Fossdal, C.G., Nagy, N., Molmann, J., Dælen, O.G. and Skrøppa, T. (2005) Climatic adaptation in Picea abies progenies is affected by the temperature during zygotic embryogenesis and seed maturation. Plant, Cell and Environment 28, 1090–1102.CrossRefGoogle Scholar
Johnsen, Ø., Kvaalen, H., Yakovlev, I.A., Dæhlen, O.G., Fossdal, C.G. and Skrøppa, T. (2009) An epigenetic memory from time of embryo development affects climatic adaptation in Norway spruce. pp. 99–107 in Gusta, L.V.; Wisniewski, M.E.; Tanino, K.K. (Eds) Plant cold hardiness. From the laboratory to the field. Wallingford, CABI.CrossRefGoogle Scholar
Jouannet, V. and Crespi, M. (2011) Long nonprotein-coding RNAs in plants. pp. 179–200 in Ugarkovic, D. (Ed.) Long non-coding RNAs, progress in molecular and subcellular biology. Berlin, Springer-Verlag.Google Scholar
Kaufmann, K., Pajoro, A. and Angenent, G.C. (2010) Regulation of transcription in plants: mechanisms controlling developmental switches. Nature Reviews Genetics 11, 830–842.CrossRefGoogle ScholarPubMed
Kinlaw, C.S. and Neale, D.B. (1997) Complex gene families in pine genomes. Trends in Plant Science 2, 356–359.CrossRefGoogle Scholar
Klevebring, D., Street, N., Fahlgren, N., Kasschau, K., Carrington, J., Lundeberg, J. and Jansson, S. (2009) Genome-wide profiling of Populus small RNAs. BMC Genomics 10, 620.CrossRefGoogle ScholarPubMed
Kohler, C. and Makarevich, G. (2006) Epigenetic mechanisms governing seed development in plants. EMBO Report 7, 1223–1227.CrossRefGoogle ScholarPubMed
Kohmann, K. and Johnsen, Ø. (1994) The timing of bud set in seedlings of Picea abies from seed crops of a cool versus a warm spring and summer. Silvae Genetica 43, 329–333.Google Scholar
Kouzarides, T. (2007) Chromatin modifications and their function. Cell 128, 693–705.CrossRefGoogle ScholarPubMed
Kovalchuk, I., Abramov, V., Pogribny, I. and Kovalchuk, O. (2004) Molecular aspects of plant adaptation to life in the Chernobyl zone. Plant Physiology 135, 357–363.CrossRefGoogle ScholarPubMed
Kvaalen, H. and Johnsen, O. (2008) Timing of bud set in Picea abies is regulated by a memory of temperature during zygotic and somatic embryogenesis. New Phytologist 177, 49–59.CrossRefGoogle ScholarPubMed
Law, J.A. and Jacobsen, S.E. (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Reviews Genetics 11, 204–220.CrossRefGoogle ScholarPubMed
Lee, J.-S., Smith, E. and Shilatifard, A. (2010) The language of histone crosstalk. Cell 142, 682–685.CrossRefGoogle ScholarPubMed
Lelandais-Brière, C., Sorin, C., Declerck, M., Benslimane, A., Crespi, M. and Hartmann, C. (2010) Small RNA diversity in plants and its impact in development. Current Genomics 11, 14–23.CrossRefGoogle ScholarPubMed
Li, X., Wang, X., He, K., Ma, Y., Su, N., He, H., Stolc, V., Tongprasit, W., Jin, W., Jiang, J., Terzaghi, W., Li, S. and Deng, X.W. (2008) High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell 20, 259–276.CrossRefGoogle ScholarPubMed
Lira-Medeiros, C.F., Parisod, C., Fernandes, R.A., Mata, C.S., Cardoso, M.A. and Ferreira, P.C.G. (2010) Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS ONE 5, e10326.CrossRefGoogle ScholarPubMed
Lister, R., O'Malley, R.C., Tonti-Filippini, J., Gregory, B.D., Berry, C.C., Millar, A.H. and Ecker, J.R. (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133, 523–536.CrossRefGoogle ScholarPubMed
Loidl, P. (2004) A plant dialect of the histone language. Trends in Plant Science 9, 84–90.CrossRefGoogle ScholarPubMed
Lu, S., Sun, Y.-H., Amerson, H. and Chiang, V.L. (2007) MicroRNAs in loblolly pine (Pinus taeda L.) and their association with fusiform rust gall development. The Plant Journal 51, 1077–1098.CrossRefGoogle ScholarPubMed
Magallóan, S.A. and Sanderson, M.J. (2005) Angiosperm divergence times: the effect of genes, codon positions, and time constraints. Evolution 59, 1653–1670.CrossRefGoogle Scholar
Matzke, M. and Mittelsten Scheid, O. (2006) Epigenetic regulation in plants. pp. 167–189 in Allis, C.D.; Jenuwein, T.; Reinberg, D. (Eds) Epigenetics. Cold Spring Harbor, New York, Cold Spring Harbor Laboratory Press.Google Scholar
Meagher, R.B. (2010) The evolution of epitype. Plant Cell 22, 1658–1666.CrossRefGoogle ScholarPubMed
Molinier, J., Ries, G., Zipfel, C. and Hohn, B. (2006) Transgeneration memory of stress in plants. Nature 442, 1046–1049.CrossRefGoogle ScholarPubMed
Mølmann, J.A., Asante, D.K.A., Jensen, J.B., Krane, M.N., Ernstsen, A., Junttila, O. and Olsen, J.E. (2005) Low night temperature and inhibition of gibberellin biosynthesis override phytochrome action and induce bud set and cold acclimation, but not dormancy in phya overexpressors and wild-type of hybrid aspen. Plant, Cell and Environment 28, 1579–1588.CrossRefGoogle Scholar
Mølmann, J.A., Junttila, O., Johnsen, Ø. and Olsen, J.E. (2006) Effects of red, far-red and blue light in maintaining growth in latitudinal populations of Norway spruce (Picea abies). Plant, Cell and Environment 29, 166–172.CrossRefGoogle ScholarPubMed
Monteuuis, O., Doulbeau, S. and Verdeil, J.-L. (2008) DNA methylation in different origin clonal offspring from a mature Sequoiadendron giganteum genotype. Trees – Structure and Function 22, 779–784.CrossRefGoogle Scholar
Morin, R.D., Aksay, G., Dolgosheina, E., Ebhardt, H.A., Magrini, V., Mardis, E.R., Sahinalp, S.C. and Unrau, P.J. (2008) Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Research 18, 571–584.CrossRefGoogle ScholarPubMed
Morse, A.M., Peterson, D.G., Islam-Faridi, M.N., Smith, K.E., Magbanua, Z., Garcia, S.A., Kubisiak, T.L., Amerson, H.V., Carlson, J.E., Nelson, C.D. and Davis, J.M. (2009) Evolution of genome size and complexity in Pinus. PLoS ONE 4, e4332.CrossRefGoogle ScholarPubMed
Murray, M.G., Peters, D.L. and Thompson, W.F. (1981) Ancient repeated sequences in the pea and mung bean genomes and implications for genome evolution. Journal of Molecular Evolution 17, 31–42.CrossRefGoogle Scholar
OECD (2011) OECD forest seed and plant scheme. 2011 Rules and regulations. Paris, OECD, p. 42.Google Scholar
Oh, T.J., Wartell, R.M., Cairney, J. and Pullman, G.S. (2008) Evidence for stage-specific modulation of specific microRNAs (miRNAs) and miRNA processing components in zygotic embryo and female gametophyte of loblolly pine (Pinus taeda). New Phytologist 179, 67–80.CrossRefGoogle ScholarPubMed
Ohri, D. (2005) Climate and growth form: The consequences for genome size in plants. Plant Biology 7, 449–458.CrossRefGoogle ScholarPubMed
Olsen, J. (2010) Light and temperature sensing and signaling in induction of bud dormancy in woody plants. Plant Molecular Biology 73, 37–47.CrossRefGoogle ScholarPubMed
Olsen, J.E., Junttila, O., Nilsen, J., Eriksson, M.E., Martinussen, I., Olsson, O., Sandberg, G. and Moritz, T. (1997) Ectopic expression of oat phytochrome a in hybrid aspen changes critical daylength for growth and prevents cold acclimatization. The Plant Journal 12, 1339–1350.CrossRefGoogle Scholar
Pavangadkar, K., Thomashow, M. and Triezenberg, S. (2010) Histone dynamics and roles of histone acetyltransferases during cold-induced gene regulation in Arabidopsis. Plant Molecular Biology 74, 183–200.CrossRefGoogle ScholarPubMed
Rehfeldt, G.E., Ying, C.C., Spittlehouse, D.L. and Hamilton, D.A. (1999) Genetic responses to climate in Pinus contorta: niche breadth, climate change, and reforestation. Ecological Monographs 69, 375–407.CrossRefGoogle Scholar
Rehfeldt, G.E., Tchebakova, N.M., Parfenova, Y.I., Wykoff, W.R., Kuzmina, N.A. and Milyutin, L.I. (2002) Intraspecific responses to climate in Pinus sylvestris. Global Change Biology 8, 912–929.CrossRefGoogle Scholar
Rohde, A. and Junttila, O. (2008) Remembrances of an embryo: long-term effects on phenology traits in spruce. New Phytologist 177, 2–5.CrossRefGoogle ScholarPubMed
Schmidtling, R.C. and Hipkins, V. (2004) The after-effects of reproductive environment in shortleaf pine. Forestry 77, 287–295.CrossRefGoogle Scholar
Simon, S.A. and Meyers, B.C. (2011) Small RNA-mediated epigenetic modifications in plants. Current Opinion in Plant Biology 14, 148–155.CrossRefGoogle ScholarPubMed
Skrøppa, T., Kohmann, K., Johnsen, Ø., Steffenrem, A. and Edvardsen, Ø.M. (2007) Field performance and early test results of offspring from two Norway spruce seed orchards containing clones transferred to warmer climates. Canadian Journal of Forest Research 37, 515–522.CrossRefGoogle Scholar
Skrøppa, T., Tollefsrud, M., Sperisen, C. and Johnsen, Ø. (2010) Rapid change in adaptive performance from one generation to the next in Picea abies – Central European trees in a Nordic environment. Tree Genetics and Genomes 6, 93–99.CrossRefGoogle Scholar
Slotkin, R.K. and Martienssen, R. (2007) Transposable elements and the epigenetic regulation of the genome. Nature Reviews Genetics 8, 272–285.CrossRefGoogle ScholarPubMed
Slotkin, R.K., Vaughn, M., Borges, F., Tanurdzić, M., Becker, J.D., Feijó, J.A. and Martienssen, R.A. (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136, 461–472.CrossRefGoogle ScholarPubMed
Stoehr, M.U., L'Hirondelle, S.J., Binder, W.D. and Webber, J.E. (1998) Parental environment aftereffects on germination, growth, and adaptive traits in selected spruce families. Canadian Journal of Forest Research 28, 418–426.CrossRefGoogle Scholar
Størmer, F. and Wielgolaski, F. (2010) Are magnetite and ferritin involved in plant memory? Reviews in Environmental Science and Biotechnology 9, 105–107.CrossRefGoogle Scholar
Sultan, S.E. (2000) Phenotypic plasticity for plant development, function and life history. Trends in Plant Science 5, 537–542.CrossRefGoogle ScholarPubMed
Sung, S. and Amasino, R.M. (2004) Vernalization and epigenetics: how plants remember winter. Current Opinion in Plant Biology 7, 4–10.CrossRefGoogle ScholarPubMed
Sung, S. and Amasino, R.M. (2006) Molecular genetic studies of the memory of winter. Journal of Experimental Botany 57, 3369–3377.CrossRefGoogle ScholarPubMed
Swiezewski, S., Liu, F., Magusin, A. and Dean, C. (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis polycomb target. Nature 462, 799–802.CrossRefGoogle ScholarPubMed
Tanino, K., Kalcsits, L., Silim, S., Kendall, E. and Gray, G. (2010) Temperature-driven plasticity in growth cessation and dormancy development in deciduous woody plants: a working hypothesis suggesting how molecular and cellular function is affected by temperature during dormancy induction. Plant Molecular Biology 73, 49–65.CrossRefGoogle ScholarPubMed
Trewavas, A. (2009) What is plant behaviour? Plant, Cell and Environment 32, 606–616.CrossRefGoogle ScholarPubMed
Turck, F. and Coupland, G. (2011) When vernalization makes sense. Science 331, 36–37.CrossRefGoogle ScholarPubMed
Valledor, L., Hasbún, R., Meijón, M., Rodríguez, J., Santamaría, E., Viejo, M., Berdasco, M., Feito, I., Fraga, M., Cañal, M.J. and Rodríguez, R. (2007) Involvement of DNA methylation in tree development and micropropagation. Plant Cell, Tissue and Organ Culture 91, 75–86.CrossRefGoogle Scholar
Valledor, L., Meijón, M., Hasbún, R., Cañal, M.J. and Rodríguez, R. (2010) Variations in DNA methylation, acetylated histone h4, and methylated histone h3 during Pinus radiata needle maturation in relation to the loss of in vitro organogenic capability. Journal of Plant Physiology 167, 351–357.CrossRefGoogle Scholar
Vázquez-Lobo, A., Carlsbecker, A., Vergara-Silva, F., Alvarez-Buylla, E.R., Piñero, D. and Engström, P. (2007) Characterization of the expression patterns of LEAFY/FLORICAULA and NEEDLY orthologs in female and male cones of the conifer genera Picea, Podocarpus, and Taxus: implications for current evo-devo hypotheses for gymnosperms. Evolution and Development 9, 446–459.CrossRefGoogle ScholarPubMed
Viejo, M., Rodríguez, R., Valledor, L., Pérez, M., Cañal, M. and Hasbún, R. (2010) DNA methylation during sexual embryogenesis and implications on the induction of somatic embryogenesis in Castanea sativa Miller. Sexual Plant Reproduction 23, 315–323.CrossRefGoogle ScholarPubMed
Wagner, D. (2003) Chromatin regulation of plant development. Current Opinion in Plant Biology 6, 20–28.CrossRefGoogle ScholarPubMed
Wang, X., Elling, A.A., Li, X., Li, N., Peng, Z., He, G., Sun, H., Qi, Y., Liu, X.S. and Deng, X.W. (2009) Genome-wide and organ-specific landscapes of epigenetic modifications and their relationships to mRNA and small RNA transcriptomes in maize. Plant Cell 21, 1053–1069.CrossRefGoogle ScholarPubMed
Webber, J., Ott, P., Owens, J. and Binder, W. (2005) Elevated temperature during reproductive development affects cone traits and progeny performance in Picea glauca–Engelmannii complex. Tree Physiology 25, 1219–1227.CrossRefGoogle Scholar
Yakovlev, I.A., Fossdal, C.G. and Johnsen, Ø. (2010) MicroRNAs, the epigenetic memory and climatic adaptation in Norway spruce. New Phytologist 187, 1154–1169.CrossRefGoogle ScholarPubMed
Yakovlev, I.A., Asante, D.K.A., Fossdal, C.G., Junttila, O. and Johnsen, Ø. (2011) Differential gene expression related to an epigenetic memory affecting climatic adaptation in Norway spruce. Plant Science 180, 132–139.CrossRefGoogle Scholar